Abstract

The aim of this study was to evaluate the prevalence of endoparasites in domestic cats (Felis catus) in the city of Sousa, state of Paraíba, Northeast Brazil. A total of 207 samples of fresh feces were randomly collected from domestic and semi-domiciled cats. The samples were analyzed by simple centrifugation and centrifuge-flotation in sucrose solution for the diagnosis of helminth eggs and enteric protozoan oocysts and cysts. Epidemiological information was obtained to determine risk factors related to infections. Among the samples collected, 81.6% (169/207; 95% CI: 77.4-83.8) were positive for at least one parasite genus. Ancylostoma spp. was the most prevalent, at 67.1% (139/207), followed by Taenia spp. at 28.5% (59/207), and Spirometra spp. and Platynosomum sp., both at 17.3% (36/207). The variables associated with helminth infection were a historic lack of deworming (Odds ratio = 12.25) and the presence of dry fur (Odds ratio = 2.15). No risk factors were observed for enteric protozoa infection. This study demonstrated a high prevalence of endoparasites in domestic cats in the city of Sousa, state of Paraíba, and associated risk factors, thus establishing an overview of the main helminths and protozoa that affect cats in this region.

Keywords:
Ancylostoma spp.; helminths; protozoa; one health; Spirometra spp.; zoonosis

Resumo

O objetivo deste estudo foi avaliar a prevalência de endoparasitos em felinos domésticos (Felis catus) na cidade de Sousa, estado da Paraíba, Nordeste do Brasil. Foram coletadas 207 amostras de fezes frescas de gatos domiciliados e semidomiciliados, de forma aleatória. Analisaram-se as amostras por centrifugação simples e centrifugo-flutuação, em solução de sacarose para o diagnóstico de ovos de helmintos e oocistos e cistos de protozoários entéricos. Informações epidemiológicas foram obtidas para a determinação dos fatores de risco relacionados às infecções. Dentre as amostras coletadas, 81,6% (169/207; IC 95%: 77,4-83,8) foram positivas para pelo menos um gênero de parasito, sendo o mais prevalente Ancylostoma spp., com 67,1% (139/207), seguido de Taenia ssp. 28,5% (59/207), Spirometra spp. e Platynosomum sp., ambos com 17,3% (36/207). As variáveis que apresentaram associação com a infecção por helmintos foram o não histórico de vermifugações (Odds ratio = 12,25) e a presença de pelos secos (Odds ratio = 2,15). Não foram observados fatores de risco para as infecções por protozoários entéricos. Este estudo demonstrou uma alta prevalência de endoparasitos em felinos domésticos, na cidade de Sousa, Paraíba, associados ao fatores de risco, estabelecendo-se assim, um panorama dos principais helmintos e protozoários que acometem gatos nesta região.

Palavras-chave:
Ancylostoma spp.; helmintos; protozoários; saúde única; Spirometra spp.; zoonose

Introduction

Brazil has around 149.6 million pets, of which 27.1 million are cats, with a growth rate of 6% in recent years (Instituto Pet Brasil, 2022Instituto Pet Brasil. Censo Pet IPB: com alta recorde de 6% em um ano, gatos lideram crescimento de animais de estimação no Brasil [online]. São Paulo: Instituto Pet Brasil; 2022 [cited 2022 Sep 2]. Available from: https://institutopetbrasil.com/fique-por-dentro/amor-pelos-animais-impulsiona-os-negocios-2-2/
https://institutopetbrasil.com/fique-por... ). Felines play an important role in society, being part of the family environment (Abbas et al., 2022Abbas I, Al-Araby M, Elmishmishy B, El Alfy E. Gastrointestinal parasites of cats in Egypt: high prevalence high zoonotic risk. BMC Vet Res 2022; 18(1): 420. http://dx.doi.org/10.1186/s12917-022-03520-0. PMid:36447265.
http://dx.doi.org/10.1186/s12917-022-035... ). This proximity may pose risks to human health, since cats are hosts of several zoonotic parasites, which in addition to directly affecting the health of these animals may cause variable disturbances, from subclinical infections to more severe gastrointestinal alterations, such as severe diarrhea, anemia, and compromised growth. The parasites can also lead to death, mainly in young animals (Sauda et al., 2019Sauda F, Malandrucco L, De Liberato C, Perrucci S. Gastrointestinal parasites in shelter cats of central Italy. Vet Parasitol Reg Stud Reports 2019; 18: 100321. http://dx.doi.org/10.1016/j.vprsr.2019.100321. PMid:31796183.
http://dx.doi.org/10.1016/j.vprsr.2019.1... ).

Cats are susceptible to several gastrointestinal parasites, including: Ancylostoma spp., Toxocara spp., Dipylidium spp., Toxascaris spp., Strongyloides spp., Platynosomum sp., Spirometra spp. and Trichuris spp., in addition to protozoa such as Toxoplasma gondii, Cystoisospora spp., Cryptosporidium spp. and Giardia sp. (Monteiro et al., 2016Monteiro MFM, Ramos RAN, Calado AMC, Lima VFS, Ramos ICN, Tenório RFL, et al. Gastrointestinal parasites of cats in Brazil: frequency and zoonotic risk. Rev Bras Parasitol Vet 2016; 25(2): 254-257. http://dx.doi.org/10.1590/S1984-29612016019. PMid:27096530.
http://dx.doi.org/10.1590/S1984-29612016... ; Pereira et al., 2017Pereira PF, Barbosa AS, Moura APP, Vasconcellos ML, Uchôa CMA, Bastos OMP, et al. Gastrointestinal parasites in stray and shelter cats in the municipality of Rio de Janeiro, Brazil. Rev Bras Parasitol Vet 2017; 26(3): 383-388. http://dx.doi.org/10.1590/s1984-29612017024. PMid:28678896.
http://dx.doi.org/10.1590/s1984-29612017... ; Silva et al., 2023aSilva ALP, Lima EF, Silva GM Fo, Ferreira LC, Campos BA, Bison I, et al. Seroepidemiological survey of anti-Toxoplasma gondii and anti-Neospora caninum antibodies in domestic cats (Felis catus) in Rolim de Moura, State of Rondônia, North Brazil. Trop Med Infect Dis 2023a; 8(4): 220. http://dx.doi.org/10.3390/tropicalmed8040220. PMid:37104346.
http://dx.doi.org/10.3390/tropicalmed804... ). Transmission can occur via the fecal-oral route, through the skin penetration of larvae, and by ingestion of intermediate and paratenic hosts (Arruda et al., 2021Arruda IF, Ramos RCF, Barbosa AS, Abboud LCS, Reis IC, Millar PR, et al. Intestinal parasites and risk factors in dogs and cats from Rio de Janeiro, Brazil. Vet Parasitol Reg Stud Reports 2021; 24: 100552. http://dx.doi.org/10.1016/j.vprsr.2021.100552. PMid:34024369.
http://dx.doi.org/10.1016/j.vprsr.2021.1... ).

Some of these parasites can cause serious diseases in humans, as in the case of T. gondii, which can cause neurological and reproductive changes, and infects a third of the world's population (Lourido, 2019Lourido S. Toxoplasma gondii. Trends Parasitol 2019; 35(11): 944-945. http://dx.doi.org/10.1016/j.pt.2019.07.001. PMid:31345768.
http://dx.doi.org/10.1016/j.pt.2019.07.0... ). Still within the protozoa, Giardia sp. and Cryptosporidium spp. also pose a risk to public health because they are responsible for cases of human parasitic diarrhea (Taghipour et al., 2021Taghipour A, Khazaei S, Ghodsian S, Shajarizadeh M, Olfatifar M, Foroutan M, et al. Global prevalence of Cryptosporidium spp. in cats: a systematic review and meta-analysis. Res Vet Sci 2021; 137: 77-85. http://dx.doi.org/10.1016/j.rvsc.2021.04.015. PMid:33933711.
http://dx.doi.org/10.1016/j.rvsc.2021.04... ; Fusaro et al., 2022Fusaro C, Chávez-Romero YA, Prada SLG, Serrano-Silva N, Bernal JE, González-Jiménez FE, et al. Burden and epidemiology of human intestinal Giardia duodenalis infection in Colombia: a systematic review. Trop Med Infect Dis 2022; 7(10): 325. http://dx.doi.org/10.3390/tropicalmed7100325. PMid:36288066.
http://dx.doi.org/10.3390/tropicalmed710... ). The most prevalent helminths are Ancylostoma spp. and Toxocara spp. (Monteiro et al., 2016Monteiro MFM, Ramos RAN, Calado AMC, Lima VFS, Ramos ICN, Tenório RFL, et al. Gastrointestinal parasites of cats in Brazil: frequency and zoonotic risk. Rev Bras Parasitol Vet 2016; 25(2): 254-257. http://dx.doi.org/10.1590/S1984-29612016019. PMid:27096530.
http://dx.doi.org/10.1590/S1984-29612016... ), which are acquired through direct contact with the infective forms of the parasites in the environment, and through ingestion of eggs containing the infective larvae in contaminated food and water. The latter are responsible for causing cutaneous larva migrans and visceral/ocular larva migrans, respectively (Mello et al., 2022Mello CCS, Nizoli LQ, Ferraz A, Chagas BC, Azario WJD, Motta SP, et al. Soil contamination by Ancylostoma spp. and Toxocara spp. eggs in elementary school playgrounds in the extreme south of Brazil. Rev Bras Parasitol Vet 2022; 31(1): e019121. http://dx.doi.org/10.1590/s1984-29612022003. PMid:35019029.
http://dx.doi.org/10.1590/s1984-29612022... ).

Studies on the prevalence of endoparasites with an adequate sampling of domestic felines in Brazil are scarce, especially when compared to studies with dogs. This may be related, in part, to the greater difficulty in handling felines due to their temperament, which results in fewer parasitological exams (Dantas-Torres, 2020Dantas-Torres F. Toxocara prevalence in dogs and cats in Brazil. Adv Parasitol 2020; 109: 715-741. http://dx.doi.org/10.1016/bs.apar.2020.01.028. PMid:32381224.
http://dx.doi.org/10.1016/bs.apar.2020.0... ). There are no studies on the prevalence of enteric parasites that affect felines in the semi-arid region of Paraíba. In other regions of Northeast Brazil, the prevalence of entoparasites in cats ranged from 23% to 65.3% (Monteiro et al., 2016Monteiro MFM, Ramos RAN, Calado AMC, Lima VFS, Ramos ICN, Tenório RFL, et al. Gastrointestinal parasites of cats in Brazil: frequency and zoonotic risk. Rev Bras Parasitol Vet 2016; 25(2): 254-257. http://dx.doi.org/10.1590/S1984-29612016019. PMid:27096530.
http://dx.doi.org/10.1590/S1984-29612016... ; Lima et al., 2017Lima VFS, Ramos RAN, Lepold R, Borges JCG, Ferreira CD, Rinaldi L, et al. Gastrointestinal parasites in feral cats and rodents from the Fernando de Noronha Archipelago, Braver. Rev Bras Parasitol Vet 2017; 26(4): 521-524. http://dx.doi.org/10.1590/s1984-29612017066. PMid:29160359.
http://dx.doi.org/10.1590/s1984-29612017... ; Teófilo et al., 2017Teófilo T, Silva JCS, Costa AP, Prazeres DC, Torres MAO, Oliveira-Neta MD. Endoparasitas em cães e gatos diagnosticados em São Luís – Maranhão. Pubvet 2017; 11(6): 587-595. http://dx.doi.org/10.22256/pubvet.v11n6.587-595.
http://dx.doi.org/10.22256/pubvet.v11n6.... ). Thus, this study aimed to describe the prevalence and risk factors associated with helminth and enteric protozoan infections in domestic cats (Felis catus) in the semi-arid region of the State of Paraiba, Northeast Brazil.

Material and Methods

Experiment location

The research was carried out in the municipality of Sousa, State of Paraiba, Northeast Brazil (6°45'50”S; 38°13'30”W), from April to October 2022. The analyses were carried out at the Laboratory of Veterinary Parasitology of the Federal Institute of Education, Science and Technology of Paraiba, Sousa Campus.

Sampling

The calculation for simple random sampling was used to determine the minimum number of samples to be collected:

n = sample size for finite population

Z = 1.96 (normal distribution value for the 95% confidence interval)

P = 50 (expected prevalence of 50% to achieve sample maximization)

d = 10 (maximum value of the 10% absolute error to estimate proportion)

N = population size

The population size considered the cat-human ratio of 18.98, described by Canatto et al. (2012)Canatto BD, Silva EA, Bernardi F, Mendes MCNC, Paranhos NT, Dias RA. Caracterização demográfica das populações de cães e gatos supervisionados do município de São Paulo. Arq Bras Med Vet Zootec 2012; 64(6): 1515-1523. http://dx.doi.org/10.1590/S0102-09352012000600017.
http://dx.doi.org/10.1590/S0102-09352012... , page 1518. Given that the estimated population of the city of Sousa is 69,723 people (IBGE, 2022Instituto Brasileiro de Geografia e Estatística – IBGE. Estimativas da população residente, Diretoria de Pesquisas, Coordenação de População e Indicadores Sociais [online]. Rio de Janeiro: IBGE; 2022 [cited 2022 Sep 10]. Available from: https://censo2022.ibge.gov.br/panorama/?utm_source=ibge&utm_medium=home&utm_campaign=portal
https://censo2022.ibge.gov.br/panorama/?... ), a population of 3,674 cats was estimated. Thus, the minimum number of animals needed to participate in the study was 93. However, 207 samples were collected.

Sample collection

The collections were carried out in randomly domiciled cats without street access, and semi-domiciled cats with free street access, both with responsible tutors, without predilection for sex, age, or breed. In households with up to three cats, one of them was selected, and in those with more than three cats, three were collected.

The animals were immobilized according to Feitosa (2014)Feitosa FLF. Semiologia veterinária. 3rd ed. São Paulo: Roca; 2014., and fecal samples were obtained by rectum washing, using 5 mL of 1:1 saline solution (0.9% NaCl + mineral oil), using a urethral lubricated probe. The samples were stored in dry screw-top containers, identified accordingly, and refrigerated at temperatures of 2 to 8°C until the analyses, within 24 h.

Diagnosis of enteroparasites

Two techniques were used to identify evolutionary forms of gastrointestinal parasites: the simple sedimentation method (Hoffman et al., 1934Hoffman WA, Pons JA, Janer JL. The sedimentation concentration method in Schistosomiasis mansoni. P R J Public Health Trop Med 1934; 9: 283-298.) and the CFSS (centrifugation-flotation in sucrose solution) (Ogassawara et al., 1986Ogassawara S, Benassi S, Larsson CE, Hagiwara MK. Prevalência de endoparasitas em gatos na cidade de São Paulo. Rev Fac Med Vet Zootec Univ São Paulo 1986; 23(1): 39-46. http://dx.doi.org/10.11606/issn.2318-3659.v23i1p39-46.
http://dx.doi.org/10.11606/issn.2318-365... ).

Samples of 5 grams of feces and 50 mL of water were used in the simple sedimentation technique. After that, each sample was macerated, sieved, and added to a sedimentation cup, where another 50 mL of water was added to complete the cup volume, and left to rest for 30 min. Soon after, the supernatant was discarded, and another 100 mL of water was added. The sample was then left for another 30 min of rest. One or two more washes were performed until the supernatant had a light hue. For the slide preparation, the supernatant was discarded, and a drop of sediment was extracted using a Pasteur pipette, with a drop of Lugol superimposed on the coverslip. At least three slides were read to increase the probability of identifying parasitic forms as described by Tibiriça et al. (2009)Tibiriça SHC, Abramo C, Simões AS, Pinheiro IO, Ribeiro LC, Coimbra ES. Validação do número de lâminas para realização do método de sedimentação espontânea das fezes. Hu Rev 2009; 35(2): 105-110. and Alvares et al. (2021)Alvares FBV, Meireles VSRV, Silva JT, Ferreira LC, Rodrigues JA, Bezerra RA, et al. Laboratory diagnosis of mange-causing mites in dogs using a modified centrifugation-flotation technique in sucrose solution. Exp Appl Acarol 2021; 85(1): 41-48. http://dx.doi.org/10.1007/s10493-021-00659-7. PMid:34557977.
http://dx.doi.org/10.1007/s10493-021-006... .

The CFSS (centrifugation-flotation in sucrose solution) method was performed using 2 grams of feces for each 20 ml of hypersaturated sucrose solution at a density of 1.203 g/cm³. Each sample was macerated, sieved, placed in a Falcon-type centrifuge tube with a volume of 15 ml and centrifuged at 2,000 rpm for 10 min. After centrifugation, the sample was collected from the surface using a loop of Henle and deposited on the slide overlaid with a cover slip (Ogassawara et al., 1986Ogassawara S, Benassi S, Larsson CE, Hagiwara MK. Prevalência de endoparasitas em gatos na cidade de São Paulo. Rev Fac Med Vet Zootec Univ São Paulo 1986; 23(1): 39-46. http://dx.doi.org/10.11606/issn.2318-3659.v23i1p39-46.
http://dx.doi.org/10.11606/issn.2318-365... ). Three slides were taken from each sample.

To measure the evolutionary forms of the parasites, an optical microscope LAB-DM300 was used, equipped with photomicrograph software, which could obtain images with up to 3.2 million pixels. All photomicrographs were produced using 40× and 100× lenses (400× and 1,000× magnifications) and the measurements were made using the Mv Image R software tools, similar to what was described by Araújo et al. (2020)Araújo HG, Silva JT, Sarmento WF, Silva SS, Bezerra RA, Azevedo SS, et al. Diversity of enteric coccidia in pigs from the Paraíba Semiarid Region of Northeastern Brazil. Rev Bras Parasitol Vet 2020; 29(4): e009120. http://dx.doi.org/10.1590/s1984-29612020079. PMid:33053055.
http://dx.doi.org/10.1590/s1984-29612020... , Melo et al. (2022)Melo LRB, Sousa LC, Lima BA, Silva ALP, Lima EF, Ferreira LC, et al. The diversity of Eimeria spp. in cattle in the Brazilian Semiarid region. Rev Bras Parasitol Vet 2022; 31(3): e006422. http://dx.doi.org/10.1590/s1984-29612022037. PMid:35830149.
http://dx.doi.org/10.1590/s1984-29612022... and Silva et al. (2022)Silva JT, Alvares FBV, Lima EF, Silva GM Fo, Silva ALP, Lima BA, et al. Prevalence and diversity of Eimeria spp. in free-range chickens in northeastern Brazil. Front Vet Sci 2022; 9: 1031330. http://dx.doi.org/10.3389/fvets.2022.1031330. PMid:36311673.
http://dx.doi.org/10.3389/fvets.2022.103... . The microscopic diagnoses of the evolutionary forms were established based on morphometric data (Urquhart et al., 1991Urquhart GM, Armour J, Duncan JL, Dunn AM, Jennings FW. Parasitologia veterinária. Rio de Janeiro: Guanabara Koogan; 1991.; Fortes, 2004Fortes E. Parasitologia veterinária. 4th ed. São Paulo: Ícone; 2004.; Bowman & Georgi, 2009Bowman DD, Georgi JR. Georgis’ parasitology for veterinarians. St. Louis: Saunders/Elsevier; 2009.).

Epidemiological questionnaire and physical examination

During the collections, a structured epidemiological questionnaire was administered to collect information about the variables that could act as possible risk factors and to obtain information about the animals in the study. The main variables investigated were food, including feed and other foods; contact with other cats or dogs; deworming of animals; environmental cleaning; vaccinations, including anti-rabies and others; castrations; and birth history. The information obtained was entered into an electronic form prepared in the Microsoft Access® program and used in the analysis of risk factors.

General clinical assessments were also carried out to obtain information about nutritional status, hair condition, presence of secretions, attitude, motility, mucosal color, heart rate, respiratory rate, rectal temperature, degree of hydration, and palpation of lymph nodes, in addition to other information such as the presence of ectoparasites at the time of the examination.

Statistical analysis

The study of risk factors associated with infection by gastrointestinal parasites was carried out using data from epidemiological questionnaires, in two stages: univariate analysis and multivariate analysis. In the univariate analysis, each independent variable was crossed with the dependent variable (positivity), and those that presented a p-value ≤ 0.20 in the chi-square test or Fisher’s exact test (Zar, 1999Zar JH. Biostatistical analysis. 4th ed. New Jersey: Prentice-Hall; 1999.) were selected for the multivariate analysis using multiple logistic regression (Hosmer & Lemeshow, 2000Hosmer DW, Lemeshow S. Applied logistic regression. 2nd ed. New York: John Wiley & Sons; 2000. http://dx.doi.org/10.1002/0471722146.
http://dx.doi.org/10.1002/0471722146... ). This threshold for variable selection in the multivariate analysis through multiple logistic regression was chosen based on established statistical practices to ensure a broader consideration of potential predictors. This approach is in line with recommendations to include variables with p-values up to 0.20 to minimize the risk of excluding potentially important predictors in the initial stages of analysis. The final model was adjusted using the Hosmer and Lemeshow coefficient to better fit the value to p≥0.05.

The collinearity of the independent variables was determined by correlation analyses. When the correlation coefficient was < 0.9, one of the variables was eliminated according to biological plausibility (Dohoo et al., 1997Dohoo IR, Ducrot C, Fourichon C, Donald A, Hurnik D. An overview of techniques for dealing with large numbers of independent variables in epidemiologic studies. Prev Vet Med 1997; 29(3): 221-239. http://dx.doi.org/10.1016/S0167-5877(96)01074-4. PMid:9234406.
http://dx.doi.org/10.1016/S0167-5877(96)... ). The significance level adopted in the multiple analysis was 5%. The results were analyzed using the GraphPad Prism® 9.0 program.

Results

It was observed that, of the 207 fecal samples collected, 81.6% (169/207; CI: 77.4-83.8) were positive for one or more genera of parasites. The prevalence of enteric helminths was 81.6% (169/207; 95% CI: 77.4-83.8) and that of enteric protozoa was 13.04% (27/207; 95% CI: 8.4-17.6).

The most prevalent helminths were Ancylostoma spp. (Figure 1A), followed by Taenia spp. (Figure 1B), Spirometra spp. (Figure 1C), Platynosomum sp. (Figure 1D), Trichuris spp. (Figure 1E) and Physaloptera spp. (Figure 1F). The most prevalent protozoa were Cystoisospora spp. (Figure 2A), coccidial oocysts (Figure 2B) and Giardia sp. (Figure 2C). The prevalence rates of helminth and protozoan infections are detailed in Table 1.

Of the positive samples, 49.8% (83/167; 95% CI: 45.7-53.9) showed co-infection with two or more parasites. The most prevalent co-infections were Ancylostoma spp. + Taenia spp., with 23% (39/169) positivity, followed by Ancylostoma spp.+ Spirometra spp., with 11.8% (20/169). Co-infections of helminths and protozoa were 10.7% (18/169) among Ancylostoma spp. and Cystoisospora spp.

The variables that showed significance for helminth and protozoan infections in the univariate analysis (p ≤ 0.20) are described in Table 2. Subsequently, they were included in the multivariate analysis (Table 3), where the risk factors associated with helminth infection obtained were no history of deworming and the presence of dry fur. As for infection by protozoa, no associated risk factors were observed.

Discussion

There was a high prevalence (81.6%, or 169/207) of parasitized felines in the present study. In studies carried out in other Brazilian states, lower prevalence values were obtained. In Pernambuco, a prevalence of 65.1% (113/173) was obtained (Monteiro et al., 2016Monteiro MFM, Ramos RAN, Calado AMC, Lima VFS, Ramos ICN, Tenório RFL, et al. Gastrointestinal parasites of cats in Brazil: frequency and zoonotic risk. Rev Bras Parasitol Vet 2016; 25(2): 254-257. http://dx.doi.org/10.1590/S1984-29612016019. PMid:27096530.
http://dx.doi.org/10.1590/S1984-29612016... ); in São Paulo, 18.7% (91/502) (Gennari et al., 2016Gennari SM, Ferreira JIGS, Pena HFJ, Labruna MB, Azevedo SS. Frequency of gastrointestinal parasites in cats seen at the University of São Paulo Veterinary Hospital, Brazil. Rev Bras Parasitol Vet 2016; 25(4): 423-428. http://dx.doi.org/10.1590/s1984-29612016082. PMid:27925073.
http://dx.doi.org/10.1590/s1984-29612016... ); in Rio de Janeiro, 24.5% (51/208) (Arruda et al., 2021Arruda IF, Ramos RCF, Barbosa AS, Abboud LCS, Reis IC, Millar PR, et al. Intestinal parasites and risk factors in dogs and cats from Rio de Janeiro, Brazil. Vet Parasitol Reg Stud Reports 2021; 24: 100552. http://dx.doi.org/10.1016/j.vprsr.2021.100552. PMid:34024369.
http://dx.doi.org/10.1016/j.vprsr.2021.1... ); and in Rio Grande do Sul, 31.8% (108/339) (Marques et al., 2017Marques SM, Oliveira MRF, Gomes MJTM. Parasitos gastrintestinais em gatos da cidade de Porto Alegre, Rio Grande do Sul. Pubvet 2017; 11(11): 1132-1137. http://dx.doi.org/10.22256/pubvet.v11n11.1132-1137.
http://dx.doi.org/10.22256/pubvet.v11n11... ). The present study used two different diagnostic techniques, simple sedimentation and CFSS, and three slides were performed, which increased the sensitivity of the results and the high positivity.

The most prevalent parasite was Ancylostoma spp., with 67.1% positivity. Similar results were found by Monteiro et al. (2016)Monteiro MFM, Ramos RAN, Calado AMC, Lima VFS, Ramos ICN, Tenório RFL, et al. Gastrointestinal parasites of cats in Brazil: frequency and zoonotic risk. Rev Bras Parasitol Vet 2016; 25(2): 254-257. http://dx.doi.org/10.1590/S1984-29612016019. PMid:27096530.
http://dx.doi.org/10.1590/S1984-29612016... and Campos et al. (2016)Campos DR, Oliveira LC, Siqueira DF, Perin LR, Campos NC, Aptekmann KP, et al. Prevalence and risk factors associated with endoparasitosis of dogs and cats in Espírito Santo, Brazil. Acta Parasitol 2016; 61(3): 544-548. http://dx.doi.org/10.1515/ap-2016-0072. PMid:27447218.
http://dx.doi.org/10.1515/ap-2016-0072... , with 67.2% and 54%, respectively. This high prevalence may be related to the monoxene life-cycle and the high egg’s laying by female, which increases environmental contamination (Bowman et al., 2002Bowman DD, Hendrix CM, Lindsay DS, Barr SC. Feline clinical parasitology. Ames: Iowa State University Press; 2002. http://dx.doi.org/10.1002/9780470376805.
http://dx.doi.org/10.1002/9780470376805... ). This high prevalence creates a public health problem because it is a zoonosis that causes cutaneous larva migrans in humans, where infection can occur through direct contact with feces containing the infective form in the environment, such as in public squares, vacant lots and sandboxes, among other sites (Campos et al., 2016Campos DR, Oliveira LC, Siqueira DF, Perin LR, Campos NC, Aptekmann KP, et al. Prevalence and risk factors associated with endoparasitosis of dogs and cats in Espírito Santo, Brazil. Acta Parasitol 2016; 61(3): 544-548. http://dx.doi.org/10.1515/ap-2016-0072. PMid:27447218.
http://dx.doi.org/10.1515/ap-2016-0072... ).

According to Campos et al. (2016)Campos DR, Oliveira LC, Siqueira DF, Perin LR, Campos NC, Aptekmann KP, et al. Prevalence and risk factors associated with endoparasitosis of dogs and cats in Espírito Santo, Brazil. Acta Parasitol 2016; 61(3): 544-548. http://dx.doi.org/10.1515/ap-2016-0072. PMid:27447218.
http://dx.doi.org/10.1515/ap-2016-0072... , the most frequent parasites in cats are Ancylostoma spp. and Toxocara spp., which are both zoonotic. However, in this study, no animal was positive for Toxocara spp., a result that differed from those of several other studies that obtained high positivity rates (Campos et al., 2016Campos DR, Oliveira LC, Siqueira DF, Perin LR, Campos NC, Aptekmann KP, et al. Prevalence and risk factors associated with endoparasitosis of dogs and cats in Espírito Santo, Brazil. Acta Parasitol 2016; 61(3): 544-548. http://dx.doi.org/10.1515/ap-2016-0072. PMid:27447218.
http://dx.doi.org/10.1515/ap-2016-0072... ; Monteiro et al., 2016Monteiro MFM, Ramos RAN, Calado AMC, Lima VFS, Ramos ICN, Tenório RFL, et al. Gastrointestinal parasites of cats in Brazil: frequency and zoonotic risk. Rev Bras Parasitol Vet 2016; 25(2): 254-257. http://dx.doi.org/10.1590/S1984-29612016019. PMid:27096530.
http://dx.doi.org/10.1590/S1984-29612016... ; Pivoto et al., 2013Pivoto FL, Lopes LFD, Vogel FSF, Botton SV, Sangioni LA. Occurrence of gastrointestinal parasites and parasitism risk factors in domestic cats in Santa Maria, RS, Brazil. Ciênc Rural 2013; 43(8): 1453-1458. http://dx.doi.org/10.1590/S0103-84782013000800018.
http://dx.doi.org/10.1590/S0103-84782013... ). In the present study, most cats (87.4%; 181/207) were over 6 months old, which is one of the factors that can lead to low rates or the absence of positivity. According to Pereira et al. (2017)Pereira PF, Barbosa AS, Moura APP, Vasconcellos ML, Uchôa CMA, Bastos OMP, et al. Gastrointestinal parasites in stray and shelter cats in the municipality of Rio de Janeiro, Brazil. Rev Bras Parasitol Vet 2017; 26(3): 383-388. http://dx.doi.org/10.1590/s1984-29612017024. PMid:28678896.
http://dx.doi.org/10.1590/s1984-29612017... , age influences the load of eggs eliminated, as when animals become adults, the larvae tend to encyst in the tissues, thus reducing the rate of evolution to adult parasites in the small intestine. In addition, the hot semi-arid climate of the region, with a rainy season from January to May, when occurs an average of 98.6% of annual rainfall (mean of 870 mm), and a dry season from June to December, with mean temperature of 27 ºC (INMET, 2022Instituto Nacional de Meteorologia – INMET. Sousa, Paraíba [online]. Brasília: INMET; 2022 [cited 2022 Oct 15]. Available from: https://portal.inmet.gov.br [[Q5: Q5]]
https://portal.inmet.gov.br ... ), may not be suitable specifically for Toxocara spp. eggs, possibly resulting in structural instability, metabolic deactivation, and desiccation, hindering their dissemination and leading to the absence of the parasite.

The most common cestode found was Taenia spp., at 28.5%. This was a high prevalence compared to that found in other studies in Brazil. Campos et al. (2016)Campos DR, Oliveira LC, Siqueira DF, Perin LR, Campos NC, Aptekmann KP, et al. Prevalence and risk factors associated with endoparasitosis of dogs and cats in Espírito Santo, Brazil. Acta Parasitol 2016; 61(3): 544-548. http://dx.doi.org/10.1515/ap-2016-0072. PMid:27447218.
http://dx.doi.org/10.1515/ap-2016-0072... found 16%, while Stalliviere et al. (2009)Stalliviere FM, Bellato V, Souza AP, Sartor AP, Moura AB, Rosa LD. Ectoparasitos e helmintos intestinais em Felis catus domesticus, da cidade de Lages, SC, Brasil e aspectos sócioeconômicos e culturais das famílias dos proprietários dos animais. Rev Bras Parasitol Vet 2009; 18(4): 26-31. http://dx.doi.org/10.4322/rbpv.01804005. PMid:20040205.
http://dx.doi.org/10.4322/rbpv.01804005... obtained only 0.7%. Similar prevalence was observed in the United States, at 36% positivity, and in Belgium, at 28% (Vanparijs et al., 1991Vanparijs O, Hermans L, van der Flaes L. Helminth and protozoan parasites in dogs and cats in Belgium. Vet Parasitol 1991; 38(1): 67-73. http://dx.doi.org/10.1016/0304-4017(91)90010-S. PMid:2024431.
http://dx.doi.org/10.1016/0304-4017(91)9... ; Loftin et al., 2019Loftin CM, Donnett UB, Schneider LG, Varela-Stokes AS. Prevalence of endoparasites in northern Mississippi shelter cats. Vet Parasitol Reg Stud Reports 2019; 18: 100322. http://dx.doi.org/10.1016/j.vprsr.2019.100322. PMid:31796170.
http://dx.doi.org/10.1016/j.vprsr.2019.1... ). One of the factors that may have contributed to the high prevalence is the hunting behaviour, reported in 60.8% (126/207) of the animals, and thus, the potential for ingestion of intermediate hosts. According to Hoopes et al. (2015)Hoopes J, Hill JE, Polley L, Fernando C, Wagner B, Schurer J, et al. Enteric parasites of free-roaming, owned, and rural cats in prairie regions of Canada. Can Vet J 2015; 56(5): 495-501. PMid:25969584., cats that engage in hunting habits may be consuming rodents that serve as intermediate hosts for Taenia spp., potentially acquiring infections through this route.

Spirometra spp. was one of the most frequent parasites in this study, with 17.3% positivity. This was considered a high prevalence compared to those found in other studies in Brazil, in which rates ranged from 1.4 to 4.8% positivity (Ramos et al., 2013Ramos DGS, Scheremeta RGAC, Oliveira ACS, Sinkoc AL, Pacheco RC. Survey of helminth parasites of cats from the metropolitan area of Cuiabá, Mato Grosso, Brazil. Rev Bras Parasitol Vet 2013; 22(2): 201-206. http://dx.doi.org/10.1590/S1984-29612013000200040. PMid:23856737.
http://dx.doi.org/10.1590/S1984-29612013... ; Ferraz et al., 2021Ferraz A, Lima CM, Barwaldt ET, Nobre MO, Nizoli LQ. Prevalência de parasitos potencialmente zoonóticos nas proximidades das escolas urbanas do município de Pedro Osório, Rio Grande do Sul, Brasil. Acta Biomed Bras 2021; 12: 39-44. http://dx.doi.org/10.18571/acbm.216.
http://dx.doi.org/10.18571/acbm.216... ). In a systematic global study, it was observed that cats had a higher rate of infection by this parasite than dogs (Badri et al., 2022Badri M, Olfatifar M, KarimiPourSaryazdi A, Zaki L, Carvalho LMM, Harandi MF, et al. The global prevalence of Spirometra parasites in snakes, frogs, dogs, and cats: a systematic review and meta-analysis. Vet Med Sci 2022; 8(6): 2785-2805. http://dx.doi.org/10.1002/vms3.932. PMid:36084292.
http://dx.doi.org/10.1002/vms3.932... ) and that these animals play an important role in the contamination of the environment. It is worth mentioning Spirometra spp.’s zoonotic potential. It is what causes the disease Sparganosis in humans, which can be acquired through the ingestion of undercooked meat and infected water containing copepods. There is no treatment other than surgically removing the larvae (Mentz et al., 2011Mentz MB, Procianoy F, Maestri MK, Rott MB. Human ocular sparganosis in southern Brazil. Rev Inst Med Trop São Paulo 2011; 53(1): 51-53. http://dx.doi.org/10.1590/S0036-46652011000100009. PMid:21412620.
http://dx.doi.org/10.1590/S0036-46652011... ).

Another important parasite that affects the health of felines is Platynosomum sp., which was found to have a pooled global infection prevalence in domestic felines (F. catus) of 17.8% (Silva et al., 2023bSilva WI, Feitosa TF, Vilela VLR. A systematic review and meta-analysis on the global status of Platynosomum sp. (Trematoda – Dicrocoelidae) infecting domestic cats (Felis catus). Vet Parasitol 2023b; 322: 110031. http://dx.doi.org/10.1016/j.vetpar.2023.110031. PMid:37742530.
http://dx.doi.org/10.1016/j.vetpar.2023.... ), very similar to the rate obtained in this study, which was 17.3%. Studies by Lima et al. (2021b)Lima RL, Pacheco RC, Mendonça AJ, Néspoli PEB, Morita LHM, Almeida ADBPF, et al. Platynosomum fastosum in domestic cats in Cuiabá, Midwest region of Brazil. Vet Parasitol Reg Stud Reports 2021b; 24: 100582. http://dx.doi.org/10.1016/j.vprsr.2021.100582. PMid:34024362.
http://dx.doi.org/10.1016/j.vprsr.2021.1... and Lins et al. (2021)Lins SBH, Dorval MEC, Pontes ERJC, Nogueira APA, Ferreira EC, Matos MFC. Parasites of zoonotic interest detected in Felis catus domesticus in Midwestern Brazil. Ens Ciênc 2021; 25(1): 29-33. http://dx.doi.org/10.17921/1415-6938.2021v25n1p29-33.
http://dx.doi.org/10.17921/1415-6938.202... in Mato Grosso do Sul obtained higher values of 26.9% and 20.9% respectively, while in Ceará, a cross-sectional study detected 42.6%, but the form of diagnosis was necropsy (Braga et al., 2016Braga RR, Teixeira AC, Oliveira JA, Cavalcanti LPG. Prevalence of Platynosomum fastosum infection in free roaming cats in northeastern Brazil: fluke burden and grading of lesions. Vet Parasitol 2016; 227: 20-25. http://dx.doi.org/10.1016/j.vetpar.2016.07.021. PMid:27523932.
http://dx.doi.org/10.1016/j.vetpar.2016.... ). The difference between the frequencies must have been due to the method used for diagnosis and the intermittent elimination of eggs (Lima et al., 2021aLima ND, Raimundo DC, Souza VAF, Aguiar JM. Occurrence of gastrointestinal parasites in dogs and cats domiciliated in Santos, SP, Brazil. Rev Bras Parasitol Vet 2021a; 30(4): e011721. http://dx.doi.org/10.1590/s1984-29612021080.
http://dx.doi.org/10.1590/s1984-29612021... ). It is necessary to emphasize the importance of infection by this parasite in the health of cats, because clinical changes can range from asymptomatic to severe liver changes (Sobral et al., 2019Sobral MCGO, Sousa SAP, Ribeiro TMP, Galvão SR, Santos RM, Silva RA, et al. Infection by Platynosomum illiciens (= P. fastosum) in domestic cats of Araguaína, Tocantins, northern Brazil. Rev Bras Parasitol Vet 2019; 28(4): 786-789. http://dx.doi.org/10.1590/s1984-29612019070. PMid:31576973.
http://dx.doi.org/10.1590/s1984-29612019... ). These results indicate veterinarians should include this parasitosis as a differential diagnosis and perform preventive diagnoses and proper deworming.

Cystoisospora spp. was the most prevalent protozoan with 11.1% of positive selections. A superior result was found by Gennari et al. (1999)Gennari SM, Kasai N, Pena HFJ, Cortez A. Ocorrência de protozoários e helmintos em amostras de fezes de cães e gatos da cidade de São Paulo. Braz J Vet Res Anim Sci 1999; 36(2): 87-91. http://dx.doi.org/10.1590/S1413-95961999000200006.
http://dx.doi.org/10.1590/S1413-95961999... , who determined that rate to be 38.5%. Other studies carried out by Gennari et al. (2016)Gennari SM, Ferreira JIGS, Pena HFJ, Labruna MB, Azevedo SS. Frequency of gastrointestinal parasites in cats seen at the University of São Paulo Veterinary Hospital, Brazil. Rev Bras Parasitol Vet 2016; 25(4): 423-428. http://dx.doi.org/10.1590/s1984-29612016082. PMid:27925073.
http://dx.doi.org/10.1590/s1984-29612016... and Arruda et al. (2021)Arruda IF, Ramos RCF, Barbosa AS, Abboud LCS, Reis IC, Millar PR, et al. Intestinal parasites and risk factors in dogs and cats from Rio de Janeiro, Brazil. Vet Parasitol Reg Stud Reports 2021; 24: 100552. http://dx.doi.org/10.1016/j.vprsr.2021.100552. PMid:34024369.
http://dx.doi.org/10.1016/j.vprsr.2021.1... obtained prevalence rates of 4.8% and 4.6%, respectively. In other countries such as Egypt, the United States, Italy, and Greece, 9.1%, 16.5%, 10.2% and 16.4% positivity rates, respectively, were found (Symeonidou et al., 2018Symeonidou I, Gelasakis AI, Arsenopoulos K, Angelou A, Beugnet F, Papadopoulos E. Feline gastrointestinal parasitism in Greece: emergent zoonotic species and associated risk factors. Parasit Vectors 2018; 11(1): 227. http://dx.doi.org/10.1186/s13071-018-2812-x. PMid:29618378.
http://dx.doi.org/10.1186/s13071-018-281... ; Hoggard et al., 2019Hoggard KR, Jarriel DM, Bevelock TJ, Verocai GG. Prevalence survey of gastrointestinal and respiratory parasites of shelter cats in northeastern Georgia, USA. Vet Parasitol Reg Stud Reports 2019; 16: 100270. http://dx.doi.org/10.1016/j.vprsr.2019.100270. PMid:31027603.
http://dx.doi.org/10.1016/j.vprsr.2019.1... ; Genchi et al., 2021Genchi M, Vismarra A, Zanet S, Morelli S, Galuppi R, Cringoli G, et al. Prevalence and risk factors associated with cat parasites in Italy: a multicenter study. Parasit Vectors 2021; 14(1): 475. http://dx.doi.org/10.1186/s13071-021-04981-2. PMid:34526126.
http://dx.doi.org/10.1186/s13071-021-049... ; Abbas et al., 2022Abbas I, Al-Araby M, Elmishmishy B, El Alfy E. Gastrointestinal parasites of cats in Egypt: high prevalence high zoonotic risk. BMC Vet Res 2022; 18(1): 420. http://dx.doi.org/10.1186/s12917-022-03520-0. PMid:36447265.
http://dx.doi.org/10.1186/s12917-022-035... ). Cystoisospora spp. is a parasite of importance to feline health because the infection is usually asymptomatic, but in immunocompromised animals it can lead to the destruction of the intestinal epithelium, causing mild to severe diarrhea, vomiting and anorexia (Symeonidou et al., 2018Symeonidou I, Gelasakis AI, Arsenopoulos K, Angelou A, Beugnet F, Papadopoulos E. Feline gastrointestinal parasitism in Greece: emergent zoonotic species and associated risk factors. Parasit Vectors 2018; 11(1): 227. http://dx.doi.org/10.1186/s13071-018-2812-x. PMid:29618378.
http://dx.doi.org/10.1186/s13071-018-281... ).

Coccidial oocysts (10-12μm) were observed in 5 (2.4%) samples. At least three genera of coccidia with similar dimensions to those found in this study have been identified, which can be shed by cats: Toxoplasma sp., Besnoitia spp., and Hammondia spp. In the semi-arid region of the State of Paraíba, there was a high prevalence of anti-T. gondii antibodies in cats, with many animals showing high antibody titers, suggesting acute infections (Feitosa et al., 2014Feitosa TF, Vilela VLR, Dantas ES, Souto DVO, Pena HFJ, Athayde ACR, et al. Toxoplasma gondii and Neospora caninum in domestic cats from the Brazilian semi-arid: seroprevalence and risk factors. Arq Bras Med Vet Zootec 2014; 66(4): 1060-1066. http://dx.doi.org/10.1590/1678-6696.
http://dx.doi.org/10.1590/1678-6696... ; Feitosa et al., 2021Feitosa TF, Costa FTR, Ferreira LC, Silva SS, Santos A, Silva WI, et al. High rate of feline immunodeficiency virus infection in cats in the Brazilian semiarid region: occurrence, associated factors and coinfection with Toxoplasma gondii and feline leukemia virus. Comp Immunol Microbiol Infect Dis 2021; 79: 101718. http://dx.doi.org/10.1016/j.cimid.2021.101718. PMid:34794005.
http://dx.doi.org/10.1016/j.cimid.2021.1... ). However, due to the similarity between the genera, it was not possible to identify them solely based on morphological characteristics associated with the serology results in the studied region. According to Dubey & Sreekumar (2003)Dubey JP, Sreekumar C. Redescription of Hammondia hammondi and its differentiation from Toxoplasma gondii. Int J Parasitol 2003; 33(13): 1437-1453. http://dx.doi.org/10.1016/S0020-7519(03)00141-3. PMid:14572507.
http://dx.doi.org/10.1016/S0020-7519(03)... , there is no easy way to distinguish Hammondia sp. from Toxoplasma sp. oocysts in cat feces except through bioassays in mice.

One of the risk factors associated with helminth infection in the multivariate analysis was the lack of deworming history. That is, 12.5% of cats that were not dewormed had more chances of becoming infected. According to studies carried out by Beugnet et al. (2014)Beugnet F, Bourdeau P, Chalvet-Monfray K, Cozma V, Farkas R, Guillot J, et al. Parasites of domestic owned cats in Europe: co-infestations and risk factors. Parasit Vectors 2014; 7(1): 291. http://dx.doi.org/10.1186/1756-3305-7-291. PMid:24965063.
http://dx.doi.org/10.1186/1756-3305-7-29... , cats that did not receive any anthelmintic treatment had a significantly greater risk of becoming infected with helminths. In the present study, most of the animals 14% (29/207) had never undergone anti-parasitic, and all of these animals tested positive for helminth eggs, which may have contributed to the high prevalence. For Strube et al. (2019)Strube C, Neubert A, Springer A, von Samson-Himmelstjerna G. Survey of German pet owners quantifying endoparasitic infection risk and implications for deworming recommendations. Parasit Vectors 2019; 12(1): 203. http://dx.doi.org/10.1186/s13071-019-3410-2. PMid:31053079.
http://dx.doi.org/10.1186/s13071-019-341... , one of the reasons for the low adherence to deworming of animals by some tutors may be the lack of information on zoonotic risks and the potential impact on feline health.

Another factor associated with helminth infection was the presence of dry fur. Cats with this characteristic have 2.15% higher chances of being infected with helminths. The presence of dry fur can indicate a suboptimal or nutritionally inadequate health status, rendering the cat more susceptible to helminth infections due to a weakened immune system (Vojtkovská et al., 2020Vojtkovská V, Voslářová E, Večerek V. Methods of assessment of the welfare of shelter cats: a review. Animals 2020; 10(9): 1527. http://dx.doi.org/10.3390/ani10091527. PMid:32872242.
http://dx.doi.org/10.3390/ani10091527... ). It may also signify that the animals are struggling to groom themselves adequately, potentially increasing the risk of coming into contact with an environment contaminated with helminth eggs, resulting in a greater likelihood of infection.

Conclusion

There was a high prevalence of intestinal parasites in domestic cats in the city of Sousa, state of Paraíba, Northeast Brazil. This study also demonstrated the prevalence of zoonotic parasites such as Ancylostoma spp. and Spirometra spp., and served as a warning for of need to adopt adequate prophylaxis and control measures. Cats with no prior deworming history and those displaying dry fur exhibit a higher positivity rate for helminth infections.

Acknowledgements

To the Coordination for the Improvement of Higher Education Personnel (CAPES) - Scholarship grant to W.I.S.

References

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